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New insights into relationships in the tribe Leptospermeae (Myrtaceae) are presented based on phylogenetic analyses of a 6‐locus, 109‐taxon dataset comprising 98 taxa sampled from all nine genera currently recognised in tribe Leptospermeae, including 76 accessions of Leptospermum s.l., and 11 outgroups representing five related tribes. Maximum parsimony and Bayesian inference analyses of separate plastid and nuclear datasets resolved five major lineages within Leptospermum, which was found to be polyphyletic with respect to other genera in the tribe, including Homalospermum, Kunzea and Neofabricia. These results concur with relationships identified in the companion phylogenomic study of the tribe by Binks & al. We also tested congruence of ovule/seed characters with the clades and the possible synapomorphy of hemitropous ovules for Asteromyrtus + Agonis s.l. To better reflect the wide variation seen in Leptospermum s.l., the genus is here restricted to members of the clade of woody‐fruited taxa found in eastern Australia, New Zealand, the Cook Islands and Malesia. To accommodate the four distinct clades of non‐woody‐fruited taxa, Leptospermopsis is reinstated for one western Australian lineage, and three new genera Apectospermum, Aggreflorum, and Gaudium are created for the other western and two largely eastern lineages, respectively, and 45 new combinations made. A key to Leptospermum and the newly segregated genera is presented. Additionally, eight names are lectotypified. [ABSTRACT FROM AUTHOR]